Development basis of phenotypic variation in egg production in a colonial ascidian: primary oocyte production versus oocyte development.

Abstract

Colonies of the ascidian Botryllus schlosseri (a cyclical hermaphrodite) exhibit extreme variability in egg production, and there is a large genetic component to this phenotypic variation. Therefore, the developmental bases of variation among different genotypes was investigated. Colonies differing in egg production (assayed as number of eggs per asexual bud) were cultured in a common garden experiment, and buds were collected and fixed early in the reproductive cycle. The buds were serially sectioned, and the number and size of the oocytes in the developing ovaries were determined for the different genotypes. Because the buds were collected prior to the onset of vitellogenesis, they contained oocytes at the three previtellogenic stages. In reproductive colonies (>0.7 eggs per bud), there were negative relationships between the final number of eggs per bud and (1) the total number of oocytes present, (2) the number of stage 1 oocytes present, and (3) the number of stage 2 oocytes present. There was no relationship between these parameters in nonreproductive colonies (<0.3 eggs per bud). In contrast, the number of stage 3 oocytes per bud was positively correlated with the final number of eggs per bud in both reproductive and nonreproductive colonies. In reproductive animals there was a negative relationship between the total number of oocytes per bud and the percentage of oocytes at stage 3 in oogenesis. A principal component analysis revealed that a single vector equally weighted for the number of eggs per bud, the total number of oocytes per bud, and the percentage of oocytes at stage 3 accounted for 84% of the observed variation in reproductive colonies. These data indicate that the phenotypic variation in egg production among the B. schlosseri colonies in the Damariscotta River, Maine, is controlled by genetic variation in both the number of oocytes that populate developing ovaries, and the percentage of oocytes that reach stage 3 in oogenesis.